scholarly journals The ghosts of parasitism past: lingering frontline anti-brood parasite defences in a former host

2021 ◽  
Author(s):  
Matthew H J Chaumont ◽  
Naomi E Langmore ◽  
Justin A Welbergen

Abstract Coevolutionary arms races between brood parasites and hosts provide tractable systems for understanding antagonistic coevolution in nature; however, little is known about the fate of frontline antiparasite defences when the host ‘wins’ the coevolutionary arms race. By recreating bygone species-interactions, using artificial parasitism experiments, lingering defensive behaviors that evolved in the context of parasitism can be understood and may even be used to identify the unknown agent of parasitism past. Here we present the first study of this type by evaluating lingering “frontline” nest defences that have evolved to prevent egg laying in a former brood parasite host. The Australian reed warbler Acrocephalus australis, is currently not parasitized but is known to exhibit fine-tuned egg discrimination—a defensive behavior indicative of a past brood parasite-host arms race and common in closely related parasitized species. Here, using 3 D-printed models of adult brood parasites, we examined whether the Australian reed warbler also exhibits frontline defences to adult brood parasites, and whether we could use these defences to identify the warbler’s “ghost of parasitism past”. Our findings provide evidence that the Australian reed warbler readily engages in frontline defences that are considered adaptive specifically in the context of brood parasitism. However, individuals were unable to discriminate between adults of different brood parasite species at their nest. Overall, our results demonstrate that despite a relaxation in selection, defences against brood parasitism can be maintained across multiple stages of the host’s nesting cycle, and further suggest that, in accordance with previous findings, that learning may be important for fine-tuning frontline defence.

Author(s):  
Václav Jelínek ◽  
Michal Šulc ◽  
Gabriela Štětková ◽  
Marcel Honza

ABSTRACTAvian brood parasites pose a serious threat for hosts, substantially reducing their fitness which selects for the evolution of host defences. A classic example of a host frontline defence is mobbing which frequently includes contact attacking of brood parasites. Here, we investigated how the nest defence of a very aggressive great reed warbler (Acrocephalus arundinaceus) host influences the speed of egg-laying and egg-removing behaviour of its brood parasite – the common cuckoo (Cuculus canorus). We video-recorded 168 brood parasitic events at 102 active host nests and found that cuckoos avoided host mobbing in only 62% of cases. If hosts spotted the cuckoo at their nests, they almost always attacked it (in 91 of 104 cases), however, such attacks only rarely and temporarily prevented cuckoos from parasitizing (11 additional cases). When attacked, cuckoos parasitized host nests significantly faster and left them immediately. However, when not attacked, cuckoos frequently stayed at or near the nest suggesting that host aggression, rather than the risk of being spotted, influences the speed of brood parasitism in this species. Further, we found that cuckoos performed egg-removing behaviour in all parasitic events without regard to host aggression. As a result, cuckoos removed at least one egg during all brood parasitism events except those when an egg slipped from their beaks and fell back into the nest (in 9 of 73 cases). This indicates that egg-removing behaviour is not costly for the common cuckoo and is an essential part of its parasitism strategy, widening understanding of this currently unexplained behaviour.


2012 ◽  
Vol 2 (2) ◽  
pp. 217-225 ◽  
Author(s):  
Sean A. Rands

The arms race between brood parasites and their hosts has led to many different host behaviours for avoiding parasitism. Some of these behaviours are social, and require the presence of conspecifics to work effectively: in response to alarm calls, some species engage in mobbing behaviour where neighbours join nest tenants in attacking and repelling an invading brood parasite. There are risks involved for the neighbours, but it has been demonstrated that social mobbing allows individuals to learn about the presence of brood parasites in the environment, suggesting that social learning is occurring. Here, I consider whether using social signals to alert naive individuals to the presence of brood parasites is a suitable strategy, compared with sitting tight on the nest in response to the signal (which should reduce the chances of being parasitized). I also compare the efficiency of these strategies with the case where individuals fail to change behaviour in response a brood parasite. Using an individual-based simulation model, I demonstrate that both mobbing and sitting tight are effective strategies in response to a signal, and that mobbing is more effective when the chances of being parasitized increase. These results are discussed and compared with known host–brood parasite relationships.


2013 ◽  
Vol 9 (4) ◽  
pp. 20130443 ◽  
Author(s):  
William E. Feeney ◽  
Naomi E. Langmore

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus , can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180203 ◽  
Author(s):  
Jukka Suhonen ◽  
Jaakko J. Ilvonen ◽  
Tommi Nyman ◽  
Jouni Sorvari

Interspecific brood parasitism is common in many animal systems. Brood parasites enter the nests of other species and divert host resources for producing their own offspring, which can lead to strong antagonistic parasite–host coevolution. Here, we look at commonalities among social insect species that are victims of brood parasites, and use phylogenetic data and information on geographical range size to predict which species are most probably to fall victims to brood parasites in the future. In our analyses, we focus on three eusocial hymenopteran groups and their brood parasites: (i) bumblebees, (ii) Myrmica ants, and (iii) vespine and polistine wasps. In these groups, some, but not all, species are parasitized by obligate workerless inquilines that only produce reproductive-caste descendants. We find phylogenetic signals for geographical range size and the presence of parasites in bumblebees, but not in ants and wasps. Phylogenetic logistic regressions indicate that the probability of being attacked by one or more brood parasite species increases with the size of the geographical range in bumblebees, but the effect is statistically only marginally significant in ants. However, non-phylogenetic logistic regressions suggest that bumblebee species with the largest geographical range sizes may have a lower likelihood of harbouring social parasites than do hosts with medium-sized ranges. Our results provide new insights into the ecology and evolution of host–social parasite systems, and indicate that host phylogeny and geographical range size can be used to predict threats posed by social parasites, as well to design efficient conservation measures for both hosts and their parasites. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180412 ◽  
Author(s):  
M. Polačik ◽  
M. Reichard ◽  
C. Smith ◽  
R. Blažek

Interspecific brood parasitism occurs in several independent lineages of birds and social insects, putatively evolving from intraspecific brood parasitism. The cuckoo catfish, Synodontis multipunctatus , the only known obligatory non-avian brood parasite, exploits mouthbrooding cichlid fishes in Lake Tanganyika, despite the absence of parental care in its evolutionary lineage (family Mochokidae). Cuckoo catfish participate in host spawning events, with their eggs subsequently collected and brooded by parental cichlids, though they can later be selectively rejected by the host. One scenario for the origin of brood parasitism in cuckoo catfish is through predation of cichlid eggs during spawning, eventually resulting in a spatial and temporal match in oviposition by host and parasite. Here we demonstrate experimentally that, uniquely among all known brood parasites, cuckoo catfish have the capacity to re-infect their hosts at a late developmental stage following egg rejection. We show that cuckoo catfish offspring can survive outside the host buccal cavity and re-infect parental hosts at a later incubation phase by exploiting the strong parental instinct of hosts to collect stray offspring. This finding implies an alternative evolutionary origin for cuckoo catfish brood parasitism, with the parental response of host cichlids facilitating its evolution. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180196 ◽  
Author(s):  
Jessica R. Litman

Brood parasitism is a specialized form of parasitism in which the offspring of a parasite develops on the food provisions gathered by a host species for its own young. Obligate brood parasitic lineages have lost the ability to acquire provisions for their young and thus rely entirely on the location of an appropriate host to serve as a food-provider. Solitary bees provide some of the most fascinating examples of brood parasitism in animals. Most solitary bees build and provision their own nests. Some, however, usurp the nests of other species of bees. These brood parasites, or ‘cuckoo’ bees, deposit their eggs on the pollen provisions collected by a host bee for her own offspring. The provisions stored by the host bee are not sufficient to sustain the development of both the host's larva and that of the brood parasite and the parasite must kill the offspring of its host in order to obtain enough nourishment to complete its development. As a consequence, there is fierce competition between the host bee seeking to protect her nest from attack and the brood parasite seeking to avoid detection by the host in order to successfully deposit her eggs in an appropriate nest. In this paper, I review the behaviours that allow brood parasitic bees to escape detection by their hosts. Identifying these behaviours, and placing them within the general context of strategies employed by brood parasitic bees to parasitize the nests of their hosts, is key to understanding how brood parasitic lineages may have evolved from nest-building ancestors, decrypting the selective pressures that drive evolutionary transitions from one strategy to another and, more broadly, revealing how similar selective pressures in widely divergent lineages of animals have given rise to remarkably convergent behaviours. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


Author(s):  
Kristen Noel ◽  
Rodger Titman ◽  
Shawn R. Craik

Conspecific brood parasitism (CBP) has been observed in approximately half of all species of waterfowl, a philopatric group in which breeding females are frequently locally related. It has been suggested that kin selection can facilitate the evolution of CBP in waterfowl via fitness benefits for the host and parasite. One model demonstrates that discrimination of related and unrelated parasites by the host must be sufficient for kinship to promote CBP, provided that costs of brood parasitism to host fitness are sufficiently low. We parameterized the model using demographic data and behavioural observations from a population of colonial Red-breasted Mergansers (Mergus serrator (Linnaeus, 1758)) in which 47% of nests were parasitized by conspecifics. The costs of 1-3 foreign eggs to host hatching success were generally small (decline of 1.8% per additional egg). Nevertheless, model outputs revealed that brood parasites maximize their inclusive fitness by avoiding nests of relatives, primarily because of constraints on a host’s ability to detect parasites at the nest. Indeed, hosts spent <8% of the diurnal period at the nest during egg laying, a period when parasite activity is greatest. It is thus highly unlikely that relatedness and kin selection promote brood parasitism in this population.


2021 ◽  
Vol 288 (1953) ◽  
pp. 20210326
Author(s):  
Eleanor M. Caves ◽  
Tanmay Dixit ◽  
John F. R. Colebrook-Robjent ◽  
Lazaro Hamusikili ◽  
Martin Stevens ◽  
...  

In host–parasite arms races, hosts can evolve signatures of identity to enhance the detection of parasite mimics. In theory, signatures are most effective when within-individual variation is low (‘consistency’), and between-individual variation is high (‘distinctiveness’). However, empirical support for positive covariation in signature consistency and distinctiveness across species is mixed. Here, we attempt to resolve this puzzle by partitioning distinctiveness according to how it is achieved: (i) greater variation within each trait, contributing to elevated ‘ absolute distinctiveness’ or (ii) combining phenotypic traits in unpredictable combinations (‘ combinatorial distinctiveness’). We tested how consistency covaries with each type of distinctiveness by measuring variation in egg colour and pattern in two African bird families (Cisticolidae and Ploceidae) that experience mimetic brood parasitism. Contrary to predictions, parasitized species, but not unparasitized species, exhibited a negative relationship between consistency and combinatorial distinctiveness. Moreover, regardless of parasitism status, consistency was negatively correlated with absolute distinctiveness across species. Together, these results suggest that (i) selection from parasites acts on how traits combine rather than absolute variation in traits, (ii) consistency and distinctiveness are alternative rather than complementary elements of signatures and (iii) mechanistic constraints may explain the negative relationship between consistency and absolute distinctiveness across species.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180198 ◽  
Author(s):  
Ros Gloag ◽  
Madeleine Beekman

Hamilton's theory of inclusive fitness provides a framework for understanding the evolution of social behaviour between kin, including parental and alloparental care. Brood parasitism is a reproductive tactic in which parasites exploit the care of other individuals of the same species (conspecific parasitism) or different species (interspecific parasitism) to rear their brood. Here, drawing from examples in birds and social insects, we identify two insights into brood parasitism that stem from inclusive fitness theory. First, the kin structure within nests, or between neighbouring nests, can create a niche space favouring the evolution of conspecific parasitism. For example, low average relatedness within social insect nests can increase selection for reproductive cheats. Likewise, high average relatedness between adjacent nests of some birds can increase a female's tolerance of parasitism by her neighbour. Second, intrabrood conflict will be high in parasitized broods, from the perspective of both parasite and host young, relative to unparasitized broods. We also discuss offspring recognition by hosts as an example of discrimination in a kin-selected social behaviour. We conclude that the inclusive fitness framework is instructive for understanding aspects of brood parasite and host evolution. In turn, brood parasites present some unique opportunities to test the predictions of inclusive fitness theory.This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


The Auk ◽  
2005 ◽  
Vol 122 (2) ◽  
pp. 566-570
Author(s):  
Dan W. Forman

Abstract Females of some bird species “steal“ the parental care of other breeding individuals by laying eggs parasitically in their nests. In most populations, conspecific brood parasites lay parasitically before laying in their own nests. By contrast, in a young and expanding Common Moorhen (Gallinula chloropus) population, 17.4% (n = 8) of brood parasites laid parasitically when their own clutches were currently being incubated, and 13.1% (n = 6) laid parasitically when they were tending to their young. This result differs from previous data on conspecific brood parasitism in this (and other) avian species and suggests that sitespecific ecological conditions exert differing selective influences on the behavioral development of populations. The behavior adopted by individual vertebrate species may not, therefore, be rigidly fixed throughout their geographic range.


Sign in / Sign up

Export Citation Format

Share Document